ECOTROPICA 17: 71–77 2011 © Society for Tropical Ecology

SEED DISPERSAL BY THE INDIAN GREY BIROSTRIS IN EASTERN GHATS,

E. Santhoshkumar & P. Balasubramanian*

Division of Landscape Ecology, Salim Ali Centre for Ornithology and Natural History Anaikatty P.O., Coimbatore - 641 108, Tamil Nadu, India

Abstract. Among the avian frugivores in tropical forests, large have an important role in the seed dispersal. The In- dian Grey Hornbill Ocyceros birostris , one of the few larger avian in the Eastern Ghats was expected to play a key role in seed dispersal. We studied i. nest middens (i.e. the seeds deposited under the active nest), ii. seed germination trial of hornbill-dispersed seeds and iii. seedling abundance under nest trees, to assess its role in seed dispersal and forest regen- eration. Of the 3303 seeds found in the nest middens, Premna tomentosa (38.6%), Drypetes roxburghii (19.5%) and Fi- licium decipiens (12.7%) formed the predominant species. Seeds found in the nest middens were intact indicating that the is a legitimate seed disperser. Germination experiments on hornbill’s diet species indicated that the seed germination efficiency of 15 out of 16 species is enhanced after defecation. Indian Grey Hornbill’s preferred diet species such as Syzygium cumini, Premna tomentosa, Diospyros montana and Drypetes roxburghii showed higher percent of germination after defecation. The number of individuals of hornbill diet species (n= 875) was significantly higher in front of the nest cavity than behind (n= 214), confirming the Indian Grey Hornbill’s role in seed dispersal. Of the 2082 seedlings recorded under the nests, 55 percent were hornbill’s diet species. The dispersal of 26 plant species during the breeding season alone indicates that the Indian Grey Hornbill is a “pivotal” species in the forest ecosystem maintenance. Key words: Eastern Ghats, Frugivory, Figs, Indian Grey Hornbill, Seed dispersal, Seed germination.

INTRODUCTION tebrates, particularly birds, is important in determin- ing their future germination behaviour (Traveset Plant- interactions play a pivotal role in main- 2001). taining the structural and functional integrity of et al. natural ecosystems. Frugivores disperse the seeds of are the principal frugivores in many of the majority of the woody plant species in the trop- the forests which they occupy and their role in seed ics (Howe & Smallwood 1982). The seed dispersal dispersal, germination and regeneration is notable process is essential for the persistence of plant popu- (Kemp 1995, Whitney et al. 1998, Kinnaird and lations and is the fundamental mechanism for the O’Brien 2007). Among the avian frugivores in organization and maintenance of species richness in tropical forests, hornbills owing to their large size plant communities (Herrera 1984, Nathan & have an important role to play in the seed dissemina- Muller-Landau 2000). Avian fruit consumption may tion and regeneration of their food plants. Hornbills ensure plant reproductive success by effectively re- can break up and swallow large fruits, may regurgitate moving fruit pulp and disperse the seeds (Carlo et al. seeds undamaged and thus, make them ideal dispers- 2003). Frugivores affect the germination success of ers (Holbrook & Smith 2000). They are known to seeds which they either defecate or regurgitate as the travel long distances in a day in search of fruits and gastrointestinal enzymes and acids within the gut of hence, are capable of moving viable seeds to distant the birds soften the hard seed coat, thus breaking locations. The pattern of hornbill seed dispersal dur- dormancy and enhancing germination in seeds ing breeding season is very different from that of the (Fleming & Heithaus 1981, Schupp 1993). The non-breeding season. The breeding habits of horn- passage of seeds through the digestive tracts of ver- bills are unique, where the female of most species seals herself into a nest cavity and leaves only a nar- row slit through which the male passes her food * e-mail: [email protected] until the nesting period is completed. The seeds of

71 SANTHOSHKUMAR & BALASUBRAMANIAN the fruits delivered to the nest inmates are squirted area. Notable frugivores include barbets ( Megalaima out through the narrow slit and are deposited at the spp), bulbuls ( Pycnonotus spp), pigeons ( Treron spp), base of the tree trunk and these are called seed mid- orioles ( Oriolus spp) and Indian Grey Hornbill ( Ocy- dens (Kemp 1995). Seed deposition at the nest trees ceros birostris ). is a useful guide to determine the diet of hornbills in Study species. The Indian Grey Hornbill measures the breeding season (Kitamura et al. 2004). Al- 50 cm and the mean mass of male bird is 375g. It is though, studies on seed deposition at nest sites by a secondary cavity nester which nests in tree cavities Asian hornbills have been conducted (Poonswad formed naturally or excavated by primary cavity nest- et al. 1987, Kannan and James 1997, Kinnaird 1998, Mudappa 2000, Klop et al. 2000, Balasubramanian ers. Nesting period starts early in March and ends in et al. 2004, Kitamura et al. 2004), information on June. The nesting period was 87 days in average, with Indian Grey Hornbill was scanty. the female sealed in the nest cavity for an average of Indian Grey Hornbill is distributed in India, 76 days and the nestlings emerged out at an average Pakistan, Nepal & Bangladesh (Ali and Ripley 1987). of 13 days after the female emerged (Santhoshkumar It is widely distributed in the Eastern Ghats, southern and Balasubramanian 2010). Indian Grey Hornbills India and found mainly in the low elevation forests breed every year, they show high nest-site fidelity, and areas of rural cultivation. The major habitats of returning to the same nest cavity. In the study area, Indian Grey Hornbill in Eastern Ghats namely dry seventy eight percent of the nest cavities were reused deciduous forests and low-land riparian forests are by hornbills in the second year breeding season severely affected by anthropogenic activities (Balasu- (Santhoshkumar and Balasubramanian 2010). bramanian et al. 2005). In the absence of other Diet. The diet of the Indian Grey Hornbill was de- large-bodied avian frugivores including other horn- termined during the breeding season by direct obser- bill species in southern Eastern Ghats, the Indian vations at the nest and by analyzing the seeds depos- Grey Hornbill appeared to have a major role in seed ited under the nest. Due to their specialized breeding dispersal. Owing to its predominantly frugivorous habits, male hornbills need to bring loads of food to habit, the hornbill is expected to consume a wide the nest site to feed the incarcerated female and variety of fruit species, and aid in seed dispersal and chicks throughout the nesting period. Seeds of the forest regeneration. Hence, the present study was fruits consumed by the female hornbill and the made with the objective of assessing its role in seed young ones in the nest cavity are squirted out dispersal and forest regeneration. through the nest slit. These seeds and fruit remains are deposited under the nest cavity and are known as MATERIALS AND METHODS nest midden. In the present study, five different nests Study site. The study was conducted in Hasanur range per year were selected and 3 x 3 m quadrates were (11°40’12” N latitude and 77°07’ 87” E longitude) laid at the base of 10 active nest trees for the period of Sathyamangalam Forest Division, Eastern Ghats, of two years (five nests per year) and the seeds were India from June 2006 to December 2008. Elevation collected once in a week and identified by compari- of this division varies from 280 to 1698 m above sea son with seeds collected from fresh fruits. Plant level. The study area receives rainfall from both species with minute seeds (<0.2 cm) were not in- South-west and North-east monsoon, annual rainfall cluded in the seed midden count as we could not varies from 600 to 850 mm. The temperature is high count them in the field. Large and medium sized (40°C) during hot summer and low (20°C) during seeds collected from nest middens were examined for winter. It has a variety of habitats raging from dry visible physical damage. In addition to nest midden scrub to wet evergreen forest. The study site, Hasa- examination for seed identification, extended watch- nur, is a plateau which extends to 30 km² at an eleva- es were carried out at active nests, to assess the food, tion of 940 msl. Dry deciduous and riparian fringing particularly fruits utilized by hornbills during breed- semi-evergreen forests are the principal vegetation ing season. In the present case, we observed five nests types here. A total of 22 fleshy-fruited species are per year. Even though there was high nest fidelity by common in both riverine and dry deciduous forests. Indian Grey hornbills, only two of the nests observed Vitex altissima, Diospyros montana and Capparis in the first year were observed in the second year. A grandis are the dominant species. Thirty seven species total of 720 hours (360 hours per year, 72 hours per of birds are reported to consume fruits in the study nest) were spent at the hides made aside the nests for

72 SEED DISPERSAL BY INDIAN GREY HORNBILL recording fruit deliveries by males to the nest in- seedlings in front of the nest cavities and behind the mates. Observations were carried out from 0600 to nest cavities, Paired-Sample T Test was used. The 1800 at 10 nests (five nests per year). Each focal nest analyses were performed with the software SPSS 10.0 selected for observation was situated not less than for Windows. 1km away from the other nest. Germination experiment. Of the seeds of 17 plant RESULTS species collected from nest middens, seed germina- Seeds of 26 fleshy fruited species belonging to 16 tion experiments on 16 plant species, excepting families were found in the middens. Of the 26 fruit Lantana camara were conducted to compare the species, 17 had medium/large seeds (>0.2cm), 9 had germination percentage of hornbill-defecated seeds minute (<0.2cm) seeds. A total of 3303 large/medi- with controls. Lantana camara , was not included in um seeds were found. Premna tomentosa, Drypetes the experiment, as it is an exotic weed and abun- roxburghii, Filicium decipiens, Diospyros montana and dantly occurring in the study area. Control un-in- Santalum album formed the predominant large/me- gested seeds were collected from fresh ripe fruits at dium seeded species (Table 1). The nine species with the study site. Three types of seed treatments were minute seeds included Moraceae (seven Ficus spp) used for germination experiments, i. hornbill-defe- and Solanaceae (two species). No physical damage cated seeds collected from the nest middens, ii. was noticed in the seeds dispersed by the hornbills. manually depulped seeds and iii. seeds with pulp. For Germination Experiment: Of the 16 species each treatment, 10 seeds were used. Seeds were sown subjected to the germination experiment, 15 species in polythene bags filled with soil sand mixture and in the bird defecated seed sample showed enhanced placed in enclosures in a nursery. The poly-bags were germination (Fig. 1). Seedling emergence was first regularly watered and the height of the seedlings was recorded for Syzygium cumini after one week of sow- recorded every week for four months from the date ing. Later in the second and third week, seedling of sowing. emergence was noted for all the other species except Natural regeneration. The role of the Indian Grey Hornbill in regeneration of its food plants was as- TABLE 1. Per cent proportion of different seed sessed by sampling the seedling abundance in front species recorded in the hornbill nest middens. and behind the nest trees. We selected 10 nests and laid two 3 x 3 m quadrates (One quadrat each in the % of S. No. Plant species Family front and behind the nest trees) one meter away from seeds the base of the tree. These 10 were not the same nests 1. Atalantia monophylla Rutaceae 1.36 used for midden examination. Selection of 10 addi- 2. Capparis grandis Capparidaceae 1.67 tional nests was aimed to cover the entire spectrum 3. Ulmaceae 0.36 of diet plants of the hornbill. The plot behind the Celtis tetrandra nest tree was used as control. A total of 20 quadrates 4. Cordia monoica Boraginaceae 0.64 were laid for sampling seedling abundance. After the 5. Cordia obliqua Boraginaceae 0.70 rainy season, in the first week of August, all seedlings 6. Diospyros montana Ebenaceae 9.87 in the 3 m plots were counted and identified. Here 7. Drypetes roxburghii Euphorbiaceae 19.59 the number of seedlings of diet species and non-diet 8. Filicium decipiens Sapindaceae 12.75 species recorded under the 10 nest trees were 9. Lantana camara Verbenaceae 1.33 summed up respectively to find out the difference in 10. Mimusops elengi Sapotaceae 1.54 total number of diet and non-diet seedlings. 11. Pithecellobium dulce Caesalpiniaceae 0.27 Statistical analysis. Differences in the germination 12. Premna tomentosa Verbenaceae 38.66 percentage of the different treatments (defecated 13. Santalum album Santalaceae 6.81 seeds vs depulped seeds vs intact fruits) and plant 14. Strychnos potatorum Loganiaceae 1.15 species were tested for statistical significance with 15. Syzygium cumini Myrtaceae 1.36 One-way ANOVA. Tamhane’s test was used for post- hoc comparison between pairs in the group. To find 16. Vitex altissima Verbenaceae 1.21 out the statistical significance of the number of diet 17. Zizyphus mauritiana Rhamnaceae 0.73

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Santalum album , in which seedlings emerged only of the nest trees were Diospyros montana (23.9%), after the fourth week. In the bird defecated seeds Drypetes roxburghii , (17.4%), Capparis grandis (5.4%) treatment, four species showed 100 percent germina- Premna tomentosa (5.4%) and Filicium decipiens tion. Nine species in the pulp removed seed treat- (5.1%). While the number of seedlings of hornbill’s ment and four species of intact fruit treatment alone food plant species was higher in front of the nests germinated, that too in lower numbers when com- (i.e. nearly four times than the behind), the non- pared to bird defecated seeds (Fig. 1). diet species was higher behind the nest, indicating According to One-Way ANOVA, significant dif- that the nest inmates squirt out their droppings ferences were observed in the case of germination through the nest hole, which falls in front of the nest percentage of three categories of seeds experimented tree (Fig. 2). The number of seedlings of the diet (F2,9 = 6.142, P < 0.05). Tamhane’s post-hoc com- species in front of the nest was significantly higher parison mean difference values between pairs for bird than the one behind the nests (Paired-Sample T Test defecated seeds and pulp removed seeds = 30.0, bird t = 3.630, df = 38 P < 0.01). There was no significant defecated seeds and seeds with pulp = 60.0 and pulp difference for non-diet species in front and behind removed seeds and seeds with pulp = 30.0. The mean the nest (Paired-Sample T Test t = 0.412, df = 24 P percentage of seed germinated for the three treat- > 0.05). ments are follows: seeds with pulp 32.5%, pulp re- moved seeds 62.5%, bird defecated seeds 92.5%. DISCUSSION Natural regeneration. Seedlings of 24 food plant spe- The present study indicates that the Indian Grey cies were recorded beneath the nests of the Indian Hornbill is a legitimate seed disperser which aids in Grey Hornbill. Dominant diet species found in front the seed dispersal of a large number of plant species

FIG. 1. Germination percentage of different types of seeds subjected to germination experiment.

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FIG. 2. Mean number of seedlings recorded per quadrat in front and behind the hornbill nest trees (n = 10).

in the study area, enhances the germination potential Kinnaird (1998) and Kitamura et al. (2004) have of seeds of their food plant species, and ultimately reported that greater numbers of diet seedlings ger- plays a major role in forest regeneration in the East- minated in front of the nest cavities of Sulawesi ern Ghats, southern India. Red-knobbed Hornbill and Wreathed Hornbill re- The Indian Grey Hornbill has some of the gen- spectively. Further evidences of hornbills’ role in seed eral features of a legitimate seed disperser. It’s diet dispersal are available from the findings of Kita- consisted of mostly fruits, and in the nest middens, mura et al. (2008) who observed significantly regurgitated/defecated seeds were found uninjured. higher densities of hornbill diet species in the quad- Seeds of 26 plant species were dispersed by the In- rates located beneath the crown of the roosting trees dian Grey Hornbill during the breeding season. than in the quadrates located beyond the crown. Studies by Whitney et al. (1998) on Ceratogymna These studies establish the fact that the Asian horn- hornbills in Cameroon and Kinnaird and O’Brien bills are important seed dispersers in the tropical (2007) on Red-knobbed Hornbill in Indonesia pro- forest ecosystem. vide supporting evidences of hornbill’s role in seed Regeneration of hornbill’s food plants was no- dispersal. The higher rate of germination observed in ticed in all the hornbill nest sites in the study area. the case of hornbill-dispersed seeds, when compared Seed dispersal of 26 plant species including the large with the control seeds indicates that the Indian Grey seeded species such as Diospyros montana and Mimu- Hornbill enhances the germination potential of seeds sops elengi which have only a fewer seed dispersing of their food plants. Our findings of enhanced ger- species highlights that the hornbill is an important mination of seeds passing through avian gut are in seed disperser. Hornbills ( Buceros bicornis, Anthraco- confirmation with that of Whitney et al (1998) on ceros malabaricus, Tockus griseus and Ocyceros birostris ) Ceratogymna hornbills and Balasubramanian & Ma- along with bulbuls ( Pynonotus spp), barbets ( Mega- heswaran (2002) on Ocyceros laima spp), mynas ( Acridotheres tristis , Gracula reli- griseus and other birds (Ridley (1936), Mishra et al. giosa ), and Koel ( Eudynamys scolopacea ) are regarded (1987), Midya and Brahmachary (1991), Naranjo as major frugivores that are likely to play a major role et al. (2003), Nogales et al. (2005) and Robertson in seed dispersal and forest regeneration in southern et al. (2006). India (Balasubramanian and Maheswaran 2002). The occurrence of greater number of seedlings Therefore, protection of bird-dispersed trees and bird of hornbill’s diet species in front of the nests than at nesting sites are suggested in order to sustain the behind the nest in the study area indicate the Indian frugivore population and enhance the natural regen- Grey Hornbill’s role in aiding forest regeneration. eration of forests.

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ACKNOWLEDGMENTS Kinnaird, M.F. 1998. Evidences for effective seed dispersal by the Sulawesi Red-knobbed Hornbill Aceros cassidix . P.B. thanks the Ministry of Environment and Forests, Biotropica 30: 50-55. Government of India for funding this project. We are Kinnaird, M.F., and T.G. O’Brien. 2007. The ecology and thankful to Dr. P.A Azeez, Director, Salim Ali Centre conservation of Asian hornbills; farmers of the forest. for Ornithology and Natural History for the encour- The University of Chicago Press, Chicago. 315 pp. agement and the Principal Chief Conservator of Kitamura, S., Yumoto T., Poonswad, P., Noma, N., Chuai- Forests, Tamil Nadu Forest Department, Chennai for lua, P., Plongmai, K., Maruhashi, T., & C. Suckasam. granting permission to work in the forests. We thank 2004. Pattern and impact of hornbill seed dispersal at the two anonymous referees and the subject editor of nest trees in a moist evergreen forest in Thailand. Jour- this journal for their useful comments on the earlier nal of Tropical Ecology 20: 545-553. versions of the manuscript. Kitamura, S., Yumoto, T., Noma, N., Chuailua, P., Ma- ruhashi, T., Wohandee, P., & P. Poonswad. 2008. Ag- REFERENCES gregated seed dispersal by wreathed hornbills at a roost site in a moist evergreen forest of Thailand. Ecological Ali, S., & S.D. Ripley. 1987. Compact Handbook of the Research 23:943-952. Birds of India and Pakistan, Oxford University Press, Klop, E., Curio, E., & L.L. Lastimoza. 2000. Breeding New Delhi, India. 737 pp. biology, nest site characteristics and nest spacing of the Balasubramanian, P., & B. Maheswaran. 2002. Frugivory, Visayan Tarictic Hornbill Penelopides panini panini on seed dispersal and regeneration by birds in south Indi- Panny, Philippines. Bird Conservation International 10: an forests. Journal of Bombay Natural History Society 17-27. 100 (2&3): 411- 431. Midya, S., & R.L., Brahmachary. 1991. The effect of birds Balasubramanian, P., Saravanan, R., & B. Maheswaran. upon germination of Banyan ( Ficus benghalensis ) seeds. 2004. Fruit preferences of the Malabar Pied Hornbill Journal of Tropical Ecology 7: 537-538. in the , India. Bird Conservation Inter- Mishra, R.M., Bhatnagar, S., & M. Sharma. 1987. Studies national 14: S69-S79. on dispersal ecology of Azadirachta indica Juss. Geobi- Balasubramanian, P., V.S. Vijayan, S.N. Prasad, & R. Ven- os 14: 112-116. kitachalam. 2005. Status and distribution of the horn- Mudappa, D. 2000. Breeding biology of the Malabar Grey bills in the Eastern Ghats, Project Report, Salim Ali Hornbill ( Ocyceros griseus ) in Southern Western Ghats, Centre for Ornithology and Natural History, Coimba- India. Journal of the Bombay Natural History Society tore, India. 32 pp. 97(1): 15-24. Carlo, T.A., Collazo, J.A., & M.J. Groom. 2003. Avian fruit Naranjo, M.E., Rengifo, C., & J, Soriano. 2003. Effect of preferences across a Puerto Rican forested landscape: ingestion by bats and birds on seed germination of pattern consistency and implications for seed removal. Stenocereus griseus and Subpilocereus repandus (Cacta- Oecologia 134: 119–131. ceae). Journal of Tropical Ecology 19: 19-25. Fleming, T.H., and E. R. Heithaus. 1981. Frugivorous bats, Nathan, R., & H.C. Muller-Landau. 2000. Spatial patterns seed shadows and the structure of tropical forests. of seed dispersal, their determinants and consequences Biotropica 13: 45-53. for recruitment. Trends in Ecology and Evolution 15: Herrera, C.M. 1984. A study of avian frugivores, bird dis- 278–285. persed plants and their interaction in Mediterranean Nogales, M., Nieves, C., Illera, J.C., Padilla, D.P., & A. scrubland. Ecological Monographs 54 (1): 1-23. Traveset. 2005. Effect of native and alien vertebrate Holbrook, K.M., & T.B. Smith. 2000. Seed dispersal and frugivores on seed viability and germination patterns of movement patterns in two species of Ceratogymna Rubia fruticosa (Rubiaceae) in the eastern Canary Is- hornbills in a West African tropical low land forest. lands. Functional Ecology 19:3. 429-436. Oecologia 125: 249-257. Poonswad, P., Tsuji, A., & C. Ngarmpongsai. 1987. A Howe, H.F. & J. Smallwood. 1982. Ecology of seed disper- comparative study on breeding biology of sympatric sal. Annual Review of Ecology and Systematics 13: hornbill species (Bucerotidae) in Thailand with impli- 201-228. cations for breeding in captivity. Pp 250-277 in Pro- Kannan, R., & D.A. James. 1997. Breeding biology of ceedings 1987 Jean Delacour/IFCB Symposium on Great Pied Hornbill ( Buceros bicornis ) in the Western breeding birds in captivity. International Foundation Ghats of South India. Journal of the Bombay Natural for the Conservation of Birds, North Hollywood, Ca- History Society 94:(3) 451-465. lifornia, USA. Kemp, A.C. 1995. The Hornbills. Oxford University Press, Ridley, H. N. 1936. The dispersal of plants throughout the Oxford, United Kingdom. 302 pp. world. Reeve & Co., Ltd., Ashford. pp 744 pp.

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